MPV17L2 is required for ribosome assembly in mitochondria

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8500-8515

  Dalla Rosa, Ilaria ^a   Durigon, Romina ^a   Pearce, Sarah F ^b   Rorbach, Joanna ^b   Hirst, Elizabeth M A ^a   Vidoni, Sara ^b   Reyes, Aurelio ^b   Brea Calvo, Gloria ^b   Minczuk, Michal ^b   Woellhaf, Michael W ^c   Herrmann, Johannes M ^c   Huynen, Martijn A ^d   Holt, Ian J ^a   Spinazzola, Antonella ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MPV17 LIKE 2 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; BIOSYNTHESIS; CELL FRACTIONATION; CELL NUCLEUS; CONTROLLED STUDY; DNA METABOLISM; EMBRYO; EVOLUTIONARY HOMOLOGY; GENE SILENCING; HUMAN; HUMAN CELL; LARGE RIBOSOMAL SUBUNIT; MITOCHONDRIAL DNA AGGREGATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RIBOSOME; MITOCHONDRION; MONOSOME; NUCLEOID; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RIBOSOME; RIBOSOME ASSEMBLY; RNA INTERFERENCE; SMALL RIBOSOMAL SUBUNIT; SUCROSE GRADIENT;

GENE SILENCING; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL SWELLING; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; RIBOSOMES;

EID: 84905586622     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku513     Document Type: Article

References (63)

1. Calvo, S., Jain, M., Xie, X., Sheth, S.A., Chang, B., Goldberger, O.A., Spinazzola, A., Zeviani, M., Carr, S.A. and Mootha, V.K. (2006) Systematic identification of human mitochondrial disease genes through integrative genomics. Nat. Genet., 38, 576-582.
2. Zwacka, R.M., Reuter, A., Pfaff, E., Moll, J., Gorgas, K., Karasawa, M. and Weiher, H. (1994) The glomerulosclerosis gene Mpv17 encodes a peroxisomal protein producing reactive oxygen species. EMBO J., 13, 5129-5134.
3. Spinazzola, A., Viscomi, C., Fernandez-Vizarra, E., Carrara, F., D'Adamo, P., Calvo, S., Marsano, R.M., Donnini, C., Weiher, H., Strisciuglio, P. et al. (2006) MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat. Genet., 38, 570-575.
4. Garone, C., Rubio, J.C., Calvo, S.E., Naini, A., Tanji, K., Dimauro, S., Mootha, V.K. and Hirano, M. (2012) MPV17 mutations causing adult-onset multisystemic disorder with multiple mitochondrial DNA deletions. Arch. Neurol., 69, 1648-1651.
5. Blakely, E.L., Butterworth, A., Hadden, R.D., Bodi, I., He, L., McFarland, R. and Taylor, R.W. (2012) MPV17 mutation causes neuropathy and leukoencephalopathy with multiple mtDNA deletions in muscle. Neuromuscul. Disord., 22, 587-591.
6. Brosius, U., Dehmel, T. and Gartner, J. (2002) Two different targeting signals direct human peroxisomal membrane protein 22 to peroxisomes. J. Biol. Chem., 277, 774-784.
7. Kaldi, K., Diestelkotter, P., Stenbeck, G., Auerbach, S., Jakle, U., Magert, H.J., Wieland, F.T. and Just, W.W. (1993) Membrane topology of the 22 kDa integral peroxisomal membrane protein. FEBS Lett., 315, 217-222.
8. Iida, R., Yasuda, T., Tsubota, E., Takatsuka, H., Matsuki, T. and Kishi, K. (2006) Human Mpv17-like protein is localized in peroxisomes and regulates expression of antioxidant enzymes. Biochem. Biophys. Res. Commun., 344, 948-954.
9. Krick, S., Shi, S., Ju, W., Faul, C., Tsai, S.Y., Mundel, P. and Bottinger, E.P. (2008) Mpv17l protects against mitochondrial oxidative stress and apoptosis by activation of Omi/HtrA2 protease. Proc. Natl. Acad Sci. U.S.A., 105, 14106-14111.
10. Rokka, A., Antonenkov, V.D., Soininen, R., Immonen, H.L., Pirila, P.L., Bergmann, U., Sormunen, R.T., Weckstrom, M., Benz, R. and Hiltunen, J.K. (2009) Pxmp2 is a channel-forming protein in Mammalian peroxisomal membrane. PLoS One, 4, e5090.
11. Pagliarini, D.J., Calvo, S.E., Chang, B., Sheth, S.A., Vafai, S.B., Ong, S.E., Walford, G.A., Sugiana, C., Boneh, A., Chen, W.K. et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell, 134, 112-123.
12. Desjardins, P., Frost, E. and Morais, R. (1985) Ethidium bromide-induced loss of mitochondrial DNA from primary chicken embryo fibroblasts. Mol. Cell. Biol., 5, 1163-1169.
13. He, J., Cooper, H.M., Reyes, A., Di Re, M., Sembongi, H., Litwin, T.R., Gao, J., Neuman, K.C., Fearnley, I.M., Spinazzola, A. et al. (2012) Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res., 40, 6109-6121.
14. Gilquin, B., Taillebourg, E., Cherradi, N., Hubstenberger, A., Gay, O., Merle, N., Assard, N., Fauvarque, M.O., Tomohiro, S., Kuge, O. et al. (2010) The AAA+ ATPase ATAD3A controls mitochondrial dynamics at the interface of the inner and outer membranes. Mol. Cell. Biol., 30, 1984-1996.
15. Almajan, E.R., Richter, R., Paeger, L., Martinelli, P., Barth, E., Decker, T., Larsson, N.G., Kloppenburg, P., Langer, T. and Rugarli, E.I. (2012) AFG3L2 supports mitochondrial protein synthesis and Purkinje cell survival. J. Clin. Invest., 122, 4048-4058.
16. Chomyn, A. (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol., 264, 197-211.
17. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
18. Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics, 27, 1164-1165.
19. Guindon, S., Delsuc, F., Dufayard, J.F. and Gascuel, O. (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol., 537, 113-137.
20. Bauerschmitt, H., Funes, S. and Herrmann, J.M. (2008) Synthesis and sorting of mitochondrial translation products. Methods Mol. Biol., 457, 95-112.
21. Donzeau, M., Kaldi, K., Adam, A., Paschen, S., Wanner, G., Guiard, B., Bauer, M.F., Neupert, W. and Brunner, M. (2000) Tim23 links the inner and outer mitochondrial membranes. Cell, 101, 401-412.
22. Fujiki, Y., Hubbard, A.L., Fowler, S. and Lazarow, P.B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol., 93, 97-102.
23. Tiranti, V., Galimberti, C., Nijtmans, L., Bovolenta, S., Perini, M.P. and Zeviani, M. (1999) Characterization of SURF-1 expression and Surf-1p function in normal and disease conditions. Hum. Mol. Genet., 8, 2533-2540.
24. Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T., Shoubridge, E.A. and Consortium, L. (2010) LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell, 21, 1315-1323.
25. Merkwirth, C. and Langer, T. (2009) Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta, 1793, 27-32.
26. Reinhold, R., Kruger, V., Meinecke, M., Schulz, C., Schmidt, B., Grunau, S.D., Guiard, B., Wiedemann, N., van der Laan, M., Wagner, R. et al. (2012) The channel-forming Sym1 protein is transported by the TIM23 complex in a presequence-independent manner. Mol. Cell. Biol., 32, 5009-5021.
27. Trott, A. and Morano, K.A. (2004) SYM1 is the stress-induced Saccharomyces cerevisiae ortholog of the mammalian kidney disease gene Mpv17 and is required for ethanol metabolism and tolerance during heat shock. Eukaryot. Cell, 3, 620-631.
28. Kasashima, K., Sumitani, M. and Endo, H. (2011) Human mitochondrial transcription factor A is required for the segregation of mitochondrial DNA in cultured cells. Exp. Cell Res., 317, 210-220.
29. Richter, R., Rorbach, J., Pajak, A., Smith, P.M., Wessels, H.J., Huynen, M.A., Smeitink, J.A., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z.M. (2010) A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J., 29, 1116-1125.
30. Cavdar Koc, E., Burkhart, W., Blackburn, K., Moseley, A. and Spremulli, L.L. (2001) The small subunit of the mammalian mitochondrial ribosome. Identification of the full complement of ribosomal proteins present. J. Biol. Chem., 276, 19363-19374.
31. Rorbach, J., Gammage, P.A. and Minczuk, M. (2012) C7orf30 is necessary for biogenesis of the large subunit of the mitochondrial ribosome. Nucleic Acids Res., 40, 4097-4109.
32. Wanschers, B.F., Szklarczyk, R., Pajak, A., van den Brand, M.A., Gloerich, J., Rodenburg, R.J., Lightowlers, R.N., Nijtmans, L.G. and Huynen, M.A. (2012) C7orf30 specifically associates with the large subunit of the mitochondrial ribosome and is involved in translation. Nucleic Acids Res., 40, 4040-4051.
33. Fung, S., Nishimura, T., Sasarman, F. and Shoubridge, E.A. (2013) The conserved interaction of C7orf30 with MRPL14 promotes biogenesis of the mitochondrial large ribosomal subunit and mitochondrial translation. Mol. Biol. Cell, 24, 184-193.
34. He, J., Cooper, H.M., Reyes, A., Di Re, M., Kazak, L., Wood, S.R., Mao, C.C., Fearnley, I.M., Walker, J.E. and Holt, I.J. (2012) Human C4orf14 interacts with the mitochondrial nucleoid and is involved in the biogenesis of the small mitochondrial ribosomal subunit. Nucleic Acids Res., 40, 6097-6108.
35. Bruni, F., Gramegna, P., Oliveira, J.M., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z.M. (2013) REXO2 is an oligoribonuclease active in human mitochondria. PLoS One, 8, e64670.
36. Dennerlein, S., Rozanska, A., Wydro, M., Chrzanowska-Lightowlers, Z.M. and Lightowlers, R.N. (2010) Human ERAL1 is a mitochondrial RNA chaperone involved in the assembly of the 28S small mitochondrial ribosomal subunit. Biochem. J., 430, 551-558.
37. Kotani, T., Akabane, S., Takeyasu, K., Ueda, T. and Takeuchi, N. (2013) Human G-proteins, ObgH1 and Mtg1, associate with the large mitochondrial ribosome subunit and are involved in translation and assembly of respiratory complexes. Nucleic Acids Res., 41, 3713-3722.
38. Uchiumi, T., Ohgaki, K., Yagi, M., Aoki, Y., Sakai, A., Matsumoto, S. and Kang, D. (2010) ERAL1 is associated with mitochondrial ribosome and elimination of ERAL1 leads to mitochondrial dysfunction and growth retardation. Nucleic Acids Res., 38, 5554-5568.
39. Bogenhagen, D.F., Martin, D.W. and Koller, A. (2014) Initial steps in RNA processing and ribosome assembly occur at mitochondrial DNA nucleoids. Cell Metab., 19, 618-629.
40. Keil, M., Bareth, B., Woellhaf, M.W., Peleh, V., Prestele, M., Rehling, P. and Herrmann, J.M. (2012) Oxa1-ribosome complexes coordinate the assembly of cytochrome C oxidase in mitochondria. J. Biol. Chem., 287, 34484-34493.
41. Ott, M. and Herrmann, J.M. (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim. Biophys. Acta, 1803, 767-775.
42. Bauerschmitt, H., Mick, D.U., Deckers, M., Vollmer, C., Funes, S., Kehrein, K., Ott, M., Rehling, P. and Herrmann, J.M. (2010) Ribosome-binding proteins Mdm38 and Mba1 display overlapping functions for regulation of mitochondrial translation. Mol. Biol. Cell, 21, 1937-1944.
43. Frazier, A.E., Taylor, R.D., Mick, D.U., Warscheid, B., Stoepel, N., Meyer, H.E., Ryan, M.T., Guiard, B. and Rehling, P. (2006) Mdm38 interacts with ribosomes and is a component of the mitochondrial protein export machinery. J. Cell Biol., 172, 553-564.
44. Gruschke, S., Grone, K., Heublein, M., Holz, S., Israel, L., Imhof, A., Herrmann, J.M. and Ott, M. (2010) Proteins at the polypeptide tunnel exit of the yeast mitochondrial ribosome. J. Biol. Chem., 285, 19022-19028.
45. Haque, M.E., Elmore, K.B., Tripathy, A., Koc, H., Koc, E.C. and Spremulli, L.L. (2010) Properties of the C-terminal tail of human mitochondrial inner membrane protein Oxa1L and its interactions with mammalian mitochondrial ribosomes. J. Biol. Chem., 285, 28353-28362.
46. Lupo, D., Vollmer, C., Deckers, M., Mick, D.U., Tews, I., Sinning, I. and Rehling, P. (2011) Mdm38 is a 14-3-3-like receptor and associates with the protein synthesis machinery at the inner mitochondrial membrane. Traffic, 12, 1457-1466.
47. Ott, M., Prestele, M., Bauerschmitt, H., Funes, S., Bonnefoy, N. and Herrmann, J.M. (2006) Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J., 25, 1603-1610.
48. Sharma, M.R., Koc, E.C., Datta, P.P., Booth, T.M., Spremulli, L.L. and Agrawal, R.K. (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell, 115, 97-108.
49. Greber, B.J., Boehringer, D., Leitner, A., Bieri, P., Voigts-Hoffmann, F., Erzberger, J.P., Leibundgut, M., Aebersold, R. and Ban, N. (2013) Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature.505, 515-519.
50. Kim, S.J., Kwon, M.C., Ryu, M.J., Chung, H.K., Tadi, S., Kim, Y.K., Kim, J.M., Lee, S.H., Park, J.H., Kweon, G.R. et al. (2012) CRIF1 is essential for the synthesis and insertion of oxidative phosphorylation polypeptides in the mammalian mitochondrial membrane. Cell Metab., 16, 274-283.
51. Piao, L., Li, Y., Kim, S.J., Byun, H.S., Huang, S.M., Hwang, S.K., Yang, K.J., Park, K.A., Won, M., Hong, J. et al. (2009) Association of LETM1 and MRPL36 contributes to the regulation of mitochondrial ATP production and necrotic cell death. Cancer Res., 69, 3397-3404.
52. Hasegawa, A. and van der Bliek, A.M. (2007) Inverse correlation between expression of the Wolfs Hirschhorn candidate gene Letm1 and mitochondrial volume in C. elegans and in mammalian cells. Hum. Mol. Genet., 16, 2061-2071.
53. Tamai, S., Iida, H., Yokota, S., Sayano, T., Kiguchiya, S., Ishihara, N., Hayashi, J., Mihara, K. and Oka, T. (2008) Characterization of the mitochondrial protein LETM1, which maintains the mitochondrial tubular shapes and interacts with the AAA-ATPase BCS1L. J. Cell Sci., 121, 2588-2600.
54. Froschauer, E., Nowikovsky, K. and Schweyen, R.J. (2005) Electroneutral K+/H+ exchange in mitochondrial membrane vesicles involves Yol027/Letm1 proteins. Biochim. Biophys. Acta, 1711, 41-48.
55. Hashimi, H., McDonald, L., Stribrna, E. and Lukes, J. (2013) Trypanosome letm1 protein is essential for mitochondrial potassium homeostasis. J. Biol. Chem., 288, 26914-26925.
56. Tsai, M.F., Jiang, D., Zhao, L., Clapham, D. and Miller, C. (2014) Functional reconstitution of the mitochondrial Ca2+/H+ antiporter Letm1. J. Gen. Physiol., 143, 67-73.
57. Dallabona, C., Marsano, R.M., Arzuffi, P., Ghezzi, D., Mancini, P., Zeviani, M., Ferrero, I. and Donnini, C. (2010) Sym1, the yeast ortholog of the MPV17 human disease protein, is a stress-induced bioenergetic and morphogenetic mitochondrial modulator. Hum. Mol. Genet., 19, 1098-1107.
58. Schon, E.A. and Przedborski, S. (2011) Mitochondria: the next (neurode)generation. Neuron, 70, 1033-1053.
59. Kowald, A. and Kirkwood, T.B. (2014) Transcription could be the key to the selection advantage of mitochondrial deletion mutants in aging. Proc. Natl. Acad. Sci. U.S.A, 11, 2972-2977.
60. Hayes, G.R., Livingston, J.N. and Lockwood, D.H. (1991) Mapping of carbohydrate sites on the human insulin receptor. Biochem. Biophys. Res. Commun., 174, 735-741.
61. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S. and O'Shea, E.K. (2003) Global analysis of protein localization in budding yeast. Nature, 425, 686-691.
62. Waterhouse, A.M., Procter, J.B., Martin, D.M., Clamp, M. and Barton, G.J. (2009) Jalview version 2 - A multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189-1191.
63. Rice, P., Longden, I. and Bleasby, A. (2000) EMBOSS: the European molecular biology open software suite. Trends Genet., 16, 276-277.